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58. Cross-Induction of the L-Fucose System by L-Rhamnose In JOURNAL OF BACTERIOLOGY, Aug. 1987, p. 3712-3719 Vol. 169, No. 8 0021-9193/87/083712-08$02.00/0 Copyright © 1987, American Society for Microbiology Cross-Induction of the L-Fucose System by L-Rhamnose in Escherichia coli Y.-M. CHEN,1 J. F. TOBIN,2 Y. ZHU,' R. F. SCHLEIF,2 AND E. C. C. LIN'* Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115,1 and Department ofBiochemistry, Brandeis University, Waltham, Massachusetts 022542 Received 6 January 1987/Accepted 21 May 1987 Dissimilation of L-fucose as a carbon and energy source by Escherichia coli involves a permease, an isomerase, a kinase, and an aldolase encoded by the fuc regulon at minute 60.2. Utilization of L-rhamnose involves a similar set of proteins encoded by the rha operon at minute 87.7. Both pathways lead to the formation of L-lactaldehyde and dihydroxyacetone phosphate. A common NAD-linked oxidoreductase encoded by fucO serves to reduce L-lactaldehyde to L-1,2-propanediol under anaerobic growth conditions, irrespective of whether the aldehyde is derived from fucose or rhamnose. In this study it was shown that anaerobic growth on rhamnose induces expression of not only thefucO gene but also the entirefuc regulon. Rhamnose is unable to induce the fuc genes in mutants defective in rhaA (encoding L-rhamnose isomerase), rhaB (encoding L-rhamnulose kinase), rhaD (encoding L-rhamnulose 1-phosphate aldolase), rhaR (encoding the positive regulator for the rha structural genes), or fucR (encoding the positive regulator for the fuc regulon). Thus, cross-induction of the L-fucose enzymes by rhamnose requires formation of L-lactaldehyde; either the aldehyde itself or the L-fuculose 1-phosphate (known to be an effector) formed from it then interacts with the fucR-encoded protein to induce the fuc regulon. L-Fucose and L-rhamnose are dissimilated by Escherichia MATERIALS AND METHODS coli in parallel ways (Fig. 1). The trunk pathway for each compound is mediated by a permease (21; J. Power, personal Chemicals. L-Lactaldehyde was prepared by the reaction communication), an isomerase (18, 41, 44), a kinase (12, 23, of ninhydrin with D-threonine (46). L-Rhamnulose was pre- 42, 45), and an aldolase (13, 14, 17, 35, 36). The two sugars pared from a solution of L-rhamnose heated with pyridine differ in the stereoconfiguration at carbons 2 and 4, but (26). L-[U-14C]rhamnose (45 to 60 mCi per milliatom of structural differences in the intermediates disappear with carbon) was purchased from Research Products Interna- cleavage of the phosphorylated ketose by the aldolase, tional Corp., Mount Prospect, Ill. L-Fucose, L-rhamnose, yielding, in both cases, dihydroxyacetone phosphate and and D-xylose were obtained from Sigma Chemical Co., St. L-lactaldehyde. Louis, Mo. Vitamin-free casein acid hydrolysate (CAA) was Aerobically, L-lactaldehyde is converted by an NAD- from ICN Nutritional Biochemicals, Cleveland, Ohio. The linked dehydrogenase to L-lactate, which is oxidized to pyruvate kinase-L-lactate dehydrogenase mixture was from pyruvate for further metabolism (15, 39); anaerobically, Boehringer Mannheim Biochemicals, Indianapolis, Ind. 5- L-lactaldehyde is reduced to L-1,2-propanediol, which is Bromo-4-chloro-3-indolyl-,3-D-galactoside (X-Gal) was from excreted into the medium (15, 40). The sacrifice of the Bachem Inc., Torrance, Calif. All other chemicals were aldehyde as a hydrogen sink increases the portion of commercial products of reagent grade. dihydroxyacetone phosphate that can be utilized as a carbon Bacteria and phage. The E. coli strains used are described and energy source. in Table 1. Eight independent clones of strain ECL116 were The catalytic proteins in each trunk pathway and the mutagenized with ethyl methanesulfonate (28). Following corresponding positive regulatory protein are encoded by a overnight growth of the treated populations in glucose- single gene cluster: thefuc locus at minute 60.2 (1, 7, 16, 37, mineral medium, a portion of each culture was enriched in 38) and the rha locus at minute 87.7 (1, 34). The structural rhamnose-negative mutants by the streptozotocin selection genes of the fuc system appear to be organized as a regulon method (25). Survivors were plated on MacConkey agar comprising at least three operons (7, 20-22), with L-fuculose containing 1% rhamnose as the sugar. Pale-colored colonies 1-phosphate as the effector (3). The rha system responds to were screened on minimal agar containing rhamnose, fu- L-rhamnose as the effector (34). cose, or glucose. Those that failed to grow only on rhamnose A common enzyme of broad function, encoded by the ald were collected and examined for the specific nature of the gene, which is linked to neither the fuc nor the rha locus, is lesion. Deficiencies of L-rhamnose permease, L-rhamnose responsible for the dehydrogenation of L-lactaldehyde to isomerase, and L-rhamnulose kinase activities were detected L-lactate (Y.-M. Chen, Y. Zhu, and E. C. C. Lin, J. by examining cells grown on CAA in the presence of Bacteriol., in press). Likewise, the reduction of L-lactal- rhamnose. Lack of L-rhamnulose 1-phosphate aldolase ac- dehyde to L-1,2-propanediol is catalyzed by a common tivity was diagnosed by inhibition of growth on glycerol in enzyme. However, the gene encoding this enzyme, fucO, is the presence of rhamnose (excessive accumulation of a a member of thefuc regulon (5, 6, 9, 11, 15). How rhamnose phosphorylated sugar causes stasis). Impairment of the causes the induction offucO is the subject of this report. activator protein encoded by rhaC (recently resolved into two genes, rhaR and rhaS [see Results]) was revealed by pleiotropic defects in the enzymes of the rhamnose pathway * Corresponding author. (34) and by complementation with a plasmid, pJTC9, bearing 3712 VOL. 169, 1987 E. COLI L-FUCOSE SYSTEM CROSS-INDUCTION BY L-RHAMNOSE 3713 L-FUCOSE 1- 9:- - :; ¢-. - ::;I: *--.:: ::;:::.-::- 1 :. :; -::--::;:'. -;- v H ~ H f Pemrnwo H*OH HO)AOH L-FUCOSE ~~HNHO-r L-FUCULOSEJ4isomemes OH H OH OH ATPQ L-FUCOSE L-RHAMNS ADPJ;Kinosc L-FUCULOSE 1-PHOSPHATE .i t AkioAose I CH20H CH20H CHO C02 HO-C-H HO-C-H HO-C-H C=O CH3 CH3 CH3 Gee CH2-O-P DIHYDROXYACETONE L-,2-PRPANEDI L-LACTALDEHYDE 11 ---* L-LACTATEA * PHOSPHATE NAD NADH NAD NAWH A Akdduse L-RHAMNULISE 1- PHOSPHATE ADP i ATPo L-RHAMNULOSE 11/so L-RHAMNOSE 1.ffnes 70-71. ie 'I ;, 11I,. L-1,2-M .AANEDOL L-RHAMNOSE FIG. 1. Catabolic pathways for L-rhamnose and L-fuCose in E. coli. rhaR+ rhaS+ (see Construction of plasmids, below). Table 2 Strain ECL711 was obtained by transducing the rhaD62 summarizes the characterization of the rhamnose-negative mutation in strain ECL484 (by selecting for a TnJO placed mutants. Strain ECL378 (TnJO 80% linked to rha+) was used nearby) into strain ECL326. as a donor by P1 vir transduction (30) to test whether or not Growth conditions. Quantitative comparisons of enzyme the mutations in rhamnose-negative strains ECL714 (rhaB), activities were carried out with extracts of cells grown ECL715 (rhaA), ECL716 (rhaD), and ECL717 (rhaR) were anaerobically at 37°C in 150-ml flasks filled to the top with at the rha locus. Strain ECL378 was constrtucted by trans- medium, tightly capped, and gently stirred by a magnet. A ducing the TnJO from strain ECL339 (zig-l::TnJO Arha) to mineral solution (43) supplemented with CAA (0.5%), pyru- strain ECL116 (rha+) by selection on LB agar containing vate (30 mM), and thiamine (2 ,ug/ml) was used as the tetracycline and scoring for red colonies on MacConkey- noninducing medium. The inducing medium also contained rhamnose-tetracycline agar. fucose or rhamnose (0.4%). For growth of strains carrying a The following procedure was used to generate an arg plasmid vector, ampicillin (200 ,uag/ml) was added to the deletion extending into the fuc region. The arg::TnJO in medium. For selecting or scoring antibiotic resistance, am- strain ECL357 was transduced into strain ECL56, in which picillin was added to 200 ,ug/ml and tetracycline was added to all of the fucose enzymes were expressed conistitutively. A 20 ,ug/ml. For the preparation of plasmid and chromosomal Tcr Arg- Fuc+ (constitutive) transductant was used for DNA, the cells were grown to stationary phase in LB generatingfuc deletion mutants by selection against the TnJO medium. conferring tetracycline resistance (4). Strain ECL478, iden- Preparation of cell extracts and enzyme assays. Cells har- tified as a Fuc- clone on MacConkey-fucose agar, was found vested from an exponentially growing culture (150 to 200 to lack significant activities of all of the fucose enzymes and Klett units; no. 42 filter) were centrifuged and washed once was thus presumed to have sustained a deletion extending with 0.1 M potassium phosphate (pH 7.0). The final pellet from arg through the entirefuc region. To place a TnJO close was weighed and dispersed in 4 volumes of the same buffer, to the arg-fuc deletion, the following procedure was used. and the cells were disrupted (1 min/ml of suspension) in a Strain ECL289 (eno fuc+ argA::TnlO) was first selected for tube by a model 60 W ultrasonic disintegrator (MSE) while the excision of TnJO (4). A derivative obtained (eno fuc+ being chilled in a - 10°C bath. The extract was centrifuged at AargA7) was used as the recipient for transduction with a P1 100,000 x g for 2 h at 4°C, and the supernatant fraction was lysate prepared from a population with random TnJO inser- used for enzyme assays. tions in the chromosome. A Tcr Eno' transductant was in L-Fucose isomerase and L-rhamnose isomerase activities turn used as the donor of the two markers with the enofuc+ were determined from the initial rate of ketose formation by AargA7 strain as the recipient.
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